1. Neuroscience
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miR-9 regulates basal ganglia-dependent developmental vocal learning and adult vocal performance in songbirds

  1. Zhimin Shi
  2. Zoe Piccus
  3. Xiaofang Zhang
  4. Huidi Yang
  5. Hannah Jarrell
  6. Yan Ding
  7. Zhaoqian Teng
  8. Ofer Tchernichovski  Is a corresponding author
  9. XiaoChing Li  Is a corresponding author
  1. Louisiana State University School of Medicine, United States
  2. Hunter College, United States
Research Article
  • Cited 7
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Cite this article as: eLife 2018;7:e29087 doi: 10.7554/eLife.29087

Abstract

miR-9 is an evolutionarily conserved miRNA that is abundantly expressed in Area X, a basal ganglia nucleus required for vocal learning in songbirds. Here, we report that overexpression of miR-9 in Area X of juvenile zebra finches impairs developmental vocal learning, resulting in a song with syllable omission, reduced similarity to the tutor song, and altered acoustic features. miR-9 overexpression in juveniles also leads to more variable song performance in adulthood, and abolishes social context-dependent modulation of song variability. We further show that these behavioral deficits are accompanied by downregulation of FoxP1 and FoxP2, genes known to be associated with language impairments, disruption of dopamine signaling, and widespread changes in expression of genes important in circuit development and functions. These findings demonstrate a vital role for miR-9 in basal ganglia function and vocal communication, suggesting that dysregulation of miR-9 in humans may contribute to language impairments and related neurodevelopmental disorders.

Article and author information

Author details

  1. Zhimin Shi

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Zoe Piccus

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Xiaofang Zhang

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Huidi Yang

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Hannah Jarrell

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Yan Ding

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Zhaoqian Teng

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Ofer Tchernichovski

    Department of Psychology, Hunter College, New York, United States
    For correspondence
    tchernichovski@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  9. XiaoChing Li

    Neuroscience Center of Excellence, Louisiana State University School of Medicine, New Orleans, United States
    For correspondence
    xli4@lsuhsc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7544-494X

Funding

National Institute of Mental Health (R01MH105519)

  • XiaoChing Li

National Science Foundation (1258015)

  • XiaoChing Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocol (#3187) of the LSU School of Medicine.

Reviewing Editor

  1. Stephanie A White, University of California, Los Angeles, United States

Publication history

  1. Received: May 30, 2017
  2. Accepted: January 17, 2018
  3. Accepted Manuscript published: January 18, 2018 (version 1)
  4. Version of Record published: February 6, 2018 (version 2)
  5. Version of Record updated: February 15, 2018 (version 3)
  6. Version of Record updated: September 19, 2018 (version 4)

Copyright

© 2018, Shi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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